Download Pelagic predator associations: tuna and dolphins in the eastern

MARINE ECOLOGY PROGRESS SERIES
Mar Ecol Prog Ser
Vol. 458: 283–302, 2012
doi: 10.3354/meps09740
Published July 3
OPEN
ACCESS
REVIEW
Pelagic predator associations: tuna and dolphins in
the eastern tropical Pacific Ocean
Michael D. Scott1,*, Susan J. Chivers2, Robert J. Olson1, Paul C. Fiedler2, Kim Holland3
1
2
3
Inter-American Tropical Tuna Commission, 8604 La Jolla Shores Dr., La Jolla California 92037, USA
Protected Resources Division, Southwest Fisheries Science Center, National Marine Fisheries Service, NOAA,
3333 North Torrey Pines Court, La Jolla, California 92037, USA
Hawaii Institute of Marine Biology, University of Hawaii at Manoa, PO Box 1346, Coconut Island, Kaneohe, Hawaii 96744, USA
ABSTRACT: The association of yellowfin tuna and pantropical spotted dolphins in the eastern
tropical Pacific Ocean (ETP) has been exploited by tuna fishermen and has intrigued scientists for
decades, yet we still have questions about what the benefits of the association are — whether the
association is obligatory or facultative, why the tuna are most often found with spotted dolphins,
and why the species associate most strongly in the ETP. We review the hypotheses that have been
proposed to explain the bond and present results from 3 studies conducted to address these
hypotheses: a simultaneous tracking study of spotted dolphins and yellowfin tuna, a trophic interactions study comparing their prey and daily foraging patterns, and a spatial study of oceanographic features correlated with the tuna–dolphin association. These studies demonstrate that the
association is neither permanent nor obligatory and that the benefits of the association are not
based on feeding advantages. These studies do support the hypothesis that one or both species
reduce the risk of predation by forming large, mixed-species groups. The association is most
prevalent where the habitat of the tuna is compressed to the warm, shallow, surface waters of the
mixed layer by the oxygen minimum zone, a thick layer of oxygen-poor waters underlying the
mixed layer. The association has been observed in other oceans with similar oceanographic conditions, but it is most prevalent and consistent in the ETP, where the oxygen minimum zone is the
most hypoxic and extensive in the world.
KEY WORDS: Spotted dolphin · Yellowfin tuna · Tuna–dolphin bond · Spinner dolphin · ETP ·
Purse-seine fishery · Food habits · Tagging
Resale or republication not permitted without written consent of the publisher
In the eastern tropical Pacific (ETP), large mixedspecies aggregations of dolphins, tunas, and seabirds
are common. Central to these aggregations are pantropical spotted dolphins Stenella attenuata and
yellowfin tuna Thunnus albacares. Tuna fishermen
have exploited this association for many decades
because the dolphins are easier to sight at a distance
and make the tuna swimming beneath them easier to
follow and catch. In the years following World War II,
baitboat fishermen would sight dolphin herds, cued
often by the presence of seabirds overhead, and then
chum the water with live baitfish to attract tuna to the
surface and catch them with hook-and-line gear. By
the mid 1960s, however, the baitboat fishery had
largely been transformed into a purse-seine fishery,
and the dolphins were no longer used just to find the
tuna, but were actively chased and encircled to catch
the tuna (Perrin 1968, Green et al. 1972). Despite the
long history of fishing tunas associated with dolphins
and the intensive management-oriented research
on the 2 species, there are still questions about the
biological basis for the association.
*Email: [email protected]
© Inter-Research 2012 · www.int-res.com
INTRODUCTION
284
Mar Ecol Prog Ser 458: 283–302, 2012
This paper reviews what is known about the association and the hypotheses that have been proposed
to explain the association, and presents results from 3
studies that could support or contradict these hypotheses. We know that the association between tuna
and dolphins is much more prevalent in the ETP than
in other oceans (Joseph & Greenough 1979, Scott et
al. 1999). Early oceanographic studies recognized
several distinctive features of the ETP: warm surface
waters, a shallow thermocline (usually less than 60 m
deep), and a thick oxygen minimum zone just below
the thermocline (Wyrtki 1964, reviews by Fiedler &
Lavín 2006, Fiedler & Talley 2006). These features
have been thought to enhance fishing success by limiting the vertical distribution of the yellowfin tuna to
the warm mixed layer near the surface (Green 1967)
and promoting the tuna–dolphin association (Perrin
et al. 1973, 1976, Au & Perryman 1985). Fishermen
were quick to determine that tuna were found most
reliably with spotted dolphins, although they were
also sometimes caught with other dolphin species
such as spinner dolphins Stenella longirostris and
short-beaked common dolphins Delphinus delphis.
Yellowfin and skipjack Katsuwonus pelamis tunas
are schooling species that are frequently found in
large aggregations and we know that the tuna–
dolphin association is one of 3 modes of tuna aggregation in the ETP. Aggregations of the smaller yellowfin, skipjack and bigeye tuna (‘logfish’) are also
commonly found in association with natural floating
objects such as logs or with manmade fish aggregating devices (FADs) seeded by the fishermen to catch
tunas more efficiently. In addition, tuna aggregations
are often found as free-swimming schools (‘schoolfish’) that are not associated with either dolphins or
floating objects. Purse-seine fisheries around the
world typically catch schoolfish and logfish, but in the
ETP, catching tuna associated with dolphins is common, and it has been suggested that the tuna–dolphin
association may be an extension of the tendency of
small tuna to associate with floating objects (Hall et
al. 1999). The association with dolphins occurs when
the yellowfin tuna become large enough to keep pace
with the more mobile dolphins (Edwards 1992).
A number of hypotheses have been suggested to
explain why tuna and dolphins associate (see reviews
by Hammond 1981, Stuntz 1981, Allen 1985, Fréon
& Misund 1999, Fréon & Dagorn 2000). After many
years of observation and research, however, 2 main
hypotheses have emerged to explain the association:
(1) one or both species may gain direct or indirect
foraging benefits from the association, and (2) one or
both species may reduce their risk of predation.
Foraging benefits
One potential benefit of the association is that it
improves foraging success. One or both species may
benefit because their large moving aggregation may
flush prey (such as flyingfish), tuna may benefit from
the dolphins’ ability to echolocate prey at a distance,
while dolphins may benefit from the tuna’s superior
sense of smell (Norris 1978, Norris & Dohl 1980a,
Au 1991, Pryor & Kang-Schallenberger 1991, Edwards
1992, Norris et al. 1994). The association occurs
where the thermocline is shallow (Au & Pitman 1986,
Edwards 1992, Norris et al. 1994, Hall et al. 1999),
and an energetics model (Edwards 1992) predicts
that the association, if based on feeding, would most
likely occur where prey is distributed in rare, but
rich, patches. The association may be involuntary for
the dolphins because large tuna can swim faster than
the dolphins (Pryor & Kang-Schallenberger 1991,
Edwards 1992).
Temporary feeding aggregations on a common
prey by tunas and dolphins have been observed
in other waters. Near the Azores, large yellowfin
and bluefin Thunnus thynnus tunas (>100 kg) are
thought to gain advantages when feeding with common dolphins Delphinus spp. and Atlantic spotted
dolphins Stenella frontalis (Clua & Grosvalet 2001).
The dolphins foraged by herding prey fishes into a
tight ball near the surface, but the tunas tended to
break up the ball, scattering both prey and dolphins.
Groups of yellowfin tuna and spinner dolphins also
have been observed foraging together off Brazil (Sazima et al. 2006). In neither of these areas, however,
have the tunas and dolphins been observed in more
than temporary feeding aggregations.
An alternative idea, that dolphins may gain feeding advantages by associating with the tuna was proposed by Au & Pitman (1986, 1988). Tunas are known
to drive prey to the surface and many seabirds are
strongly dependent on this source of prey (Ashmole
& Ashmole 1967). The feeding advantages that seabirds gain from associating with the tuna, it is argued,
could be gained by the dolphins as well.
Protection from predators
One benefit of travelling in large groups of fish or
mammals is to reduce an individual’s risk of predation (see reviews by Brock & Riffenburgh 1960,
Hamilton 1971, Jarman 1974, Partridge 1982, Inman
& Krebs 1987). Reduced risk may be due to the dilution effect (whereby the risk is lessened by spreading
Scott et al.: Tuna–dolphin association
it over a larger number of individuals), the confusion
effect (whereby predators have increased difficulty
in tracking a potential target within a large group of
similarly colored and rapidly moving individuals),
the encounter effect (whereby a single predator
would be less likely to encounter prey that is concentrated in a few large groups rather than dispersed in
many smaller groups), and the vigilance effect
(whereby predators can be detected more readily by
integrating the senses of a large number of individuals). Large sharks and billfishes are commonly
caught in association with tunas in the ETP (Au 1991,
Hunsicker et al. 2012), and are known both to prey
on tunas and dolphins and to compete with them for
the same prey (Leatherwood et al. 1973, Scott &
Cattanach 1998, Galván-Magaña 1999, Heithaus
2001, Acevedo-Gutiérrez 2002, Maldini 2003, SantosMonteiro et al. 2006, Bocanegra-Castillo 2007, Felando & Medina 2011, Hunsicker et al. 2012). False
killer whales Pseudorca crassidens and killer whales
Orcinus orca are also known predators (Perrin &
Hohn 1994, Pitman et al. 2003). Au et al. (1999) noted
that yellowfin tuna would stop feeding to follow spotted dolphins that were attempting to avoid their
research ship and suggested that ‘fleeing with dolphins would be advantageous to tuna if, as a general
tactic, it results in escaping predators most of the
time’. Scott & Cattanach (1998) argued that, because
spotted dolphins and yellowfin tuna have many of
the same potential predators, dolphin herds in the
ETP increase during the daytime to reduce the risk
of predation, and schools of large yellowfin tuna
increase as well due to their association with the
dolphins.
Exploring the hypotheses
We conducted 3 studies in the ETP to provide information that could support or contradict these hypotheses. The first was a simultaneous tracking study
that used pressure-sensitive sonic transmitters on
tuna and radiotags and time-depth recorders (TDRs)
on dolphins to record movements and diving patterns. The second was a trophic interactions study
that examined the stomach contents of dolphins and
tunas captured together in purse-seine nets. The
third used information collected by observers aboard
tuna purse seiners on the spatial extent of the tuna–
dolphin association in relation to oceanographic
features. The results from these and previous studies could answer pivotal questions about the tuna–
dolphin association: whether the association is oblig-
285
atory for either species, which species initiates the
association, what the benefits of the association are
for one or both species, why the association primarily
occurs between large yellowfin and spotted dolphins,
and why the species associate so strongly in the ETP
and not elsewhere.
SIMULTANEOUS TRACKING
Methods
The simultaneous tracking study was conducted
during a 30 day research cruise in November to
December 1993 aboard the NOAA RV ‘McArthur’
and the chartered purse seiner ‘Convemar’. Details of
the capture, tagging, and tracking of the dolphins are
described by Scott & Chivers (2009). In summary,
tuna–dolphin aggregations were encircled by the
purse seiner. The dolphins were caught by swimmers
inside the net, placed in a raft, outfitted with radio
transmitters, and released back inside the net so that
the entire aggregation could be released from the net
together. Transmitters were mounted on plastic saddles that were attached to the dorsal fin with Delrin
pins secured by corrodible magnesium nuts; TDRs
were also incorporated into most of the dolphin transmitter packages. TDRs recorded the time and the
depth of the package every 5 s, and the data were
recovered when the dolphin was recaptured and the
package removed.
The tuna were tagged with sonic transmitters attached to flat dart heads. Three types of transmitters
were used: one type gave only horizontal movement
information (Model V3: 71 kHz, range 0.5−0.75 nautical miles (n miles), VEMCO), while the other 2 also
transmitted the ambient pressure to monitor the animals’ swimming depth (Models V7P: 50 kHz, range
0.75−1.0 n miles, and V3P: 60 kHz, range 0.5−0.75 n
miles, VEMCO). The transmitters had nominal longevities of 8 to 13 days. Swimmers used lances to implant the dart tips into the dorsal musculature of the
yellowfin tuna as they were being released from the
net. We attempted to tag 2 tuna per set, a primary focal animal with the longer range V7P tag, and a
backup animal in case the primary animal could not
be released. We attempted to release all the dolphins
and tuna together, either by the normal backdown release procedure (Coe & Sousa 1972) or by releasing
one end of the net (‘dropping the ortza’) from the
boat, creating an opening for the animals to escape.
Two tracking boats (5 to 9 m long) were rigged
with sonic- and radio-tracking gear to track both
Mar Ecol Prog Ser 458: 283–302, 2012
286
dolphins and tuna. A receiver and hydrophone
tuna came within 400 m of several other dolphin
(Models VR-60 receiver and VH-65 hydrophone,
herds the following day, including one herd accomVEMCO) were mounted on the tracking boats using
panied by feeding seabirds, but it did not join these
a system described by Holland et al. (1985). When
herds. The dolphin milled over the continental slope
sonic tracking, the pulse repetition rate of the presand 15 n miles offshore of the coast over the next 4 d.
sure-sensitive sonic transmitter was recorded and
After excluding the first 2 h of data after release from
decoded, and the position of the tracking boat, and
the net, the dolphin’s average travelling speed was
the time and depth of the tuna were recorded
9.8 km h−1 (= 6.7 knots [kn] or 2.7 m s−1; Scott &
Chivers 2009). The tuna travelled at an average
approximately every 5 s. Radiotracking receivers
speed of 7.4 km h−1 (= 4.6 kn or 2.1 m s−1) along the
were also mounted on the RV ‘McArthur’ and the
continental slope to the northwest before milling in
purse seiner. When radio-tracking from any of the
an area about 15 n miles away from the dolphin.
vessels, the position, time, heading of the vessel,
Even though Dolphin D8 and Tuna T1 were sepabearing to the dolphin, and signal strength were
rated for most of their tracks, their diving histories
recorded every 15 min. The purse seiner’s helicopter
were recorded simultaneously (Fig. 2).
allowed us to observe the behavior of the dolphins
Dolphin D9 and Tuna T3, along with about 120
and tuna and monitor changes in herd size and
spotted dolphins and a few tuna, were released
composition of the aggregation.
together at 09:46 h on 26 November 1993, but the
A SEACAT mini-CTD (Sea-Bird model SBE 19) or
tuna was tracked for only 1 h due to a malfunctionan expendable bathythermograph (XBT) was deing tracking boat. Dolphin D11 and Tuna T5 were
ployed to measure depth and temperature from the
captured together; D11 was released at 12:45 h on
RV ‘McArthur’ approximately every 4 h to a depth of
at least 200 m. A shipboard environmental data acquisition system
(SEAS) collected and processed
Table 1. Stenella attenuata and Thunnus albacares. Summary of sets and tagging
and tracking operations during 1993. VHF: 148−150 MHz radio transmitter
these data. Of particular interest
only; TDR: VHF transmitter plus a time-depth recorder; V7P: 50 kHz pressurewas the correlation of the swimming
sensitive sonic transmitter; V3P: 60 kHz pressure-sensitive sonic transmitter,
depths of the dolphins and tuna
V3: 71 kHz sonic transmitter
with the depth of the thermocline.
Date
Position
captured
Dolphins
tagged
Tuna
tagged
Comments
Results
19 Nov 17°48’N, 103°30’W
Five dolphins were tracked during the study from 1 to over 4 d during 1993 (Scott & Chivers 2009),
and 3 focal tuna were tracked for 1,
8, and 31 h. Table 1 provides details
of the capture and tracks made
when both dolphins and tuna were
tagged. These tracks allow us to
compare the horizontal and vertical
movements of the 2 species.
The longest simultaneous track
involved Dolphin D8 and Tuna T1.
These 2 animals were released
from the net together, along with
about 60 spotted dolphins and
about 100 yellowfin tuna, at 11:20 h
on 21 November 1993 (Fig. 1). The
tuna and dolphin separated 2.5 h
later and did not rejoin during the
rest of the track but remained
within 15 n miles of each other. The
D7 (TDR)
191 cm male
D7 tracked for 19 h
20 Nov 17°21’N, 103°54’W
21 Nov 18°34’N, 103°57’W
D7 recaptured
D8 (TDR)
T1 (V7P)
198 cm female ~ 25 kg
with ~1 yr calf T2 (V3P)
~ 25 kg
23 Nov 18°37’N, 104°02’W
26 Nov 18°28’N, 104°14’W
D8 recaptured
D9 (TDR)
T3 (V7P)
196 cm female ~30 kg
T4 (V3P)
~25 kg
29 Nov 18°23’N, 104°04’W
D10 (TDR)
200 cm male
30 Nov 18°21’N, 104°12’W
D11 (VHF)
175 cm male
30 Nov 18°17’N, 104°16’W
D8 tracked for 49 h
T1 tracked for 31 h
T2 not tracked
D9 tracked for 102 h
T3 tracked 1 h
T4 not tracked
D10 tracked 32 h
T5 (V7P)
~10 kg
T6 (V3)
~10 kg
D11 tracked 11 h
T5 tracked 8 h
T6 not tracked
Recaptured D9
Scott et al.: Tuna–dolphin association
Fig. 1. Stenella attenuata and Thunnus albacares. (a) Movements of Dolphin D8 and Tuna T1 tracked simultaneously
during 21 to 23 November 1993 off the Pacific coast of Mexico and (b) movements of Tuna T5 and Dolphins D10 and
D11 tracked during 29 November to 1 December 1993. T5
and D11 were captured together off the Pacific coast of Mexico but released 15 min apart; D10 was tagged and released
the previous day. Bottom contours shown in meters. Capture
locations are indicated by black circles
30 November (Fig. 1), but T5 could not be backed
out of the net with the dolphins and had to be
released 15 min later. The dolphin was released
with 29 spotted and 21 spinner dolphins, and the
287
tuna was released with about 600 tuna. The tuna
did not rejoin the original dolphin herd, but was
close to a group of dolphins from 19:00 to 22:00 h,
as evidenced by the echolocation sounds heard
through the tracking hydrophone and the visual
observations of rapidly swimming and jumping dolphins. The tuna’s signal was lost at about 22:00 h
when the weather worsened and the tuna’s speed
increased. The average speed of Dolphin D11 was
9.3 km h−1 (= 5.8 kn or 2.6 m s−1; Scott & Chivers
2009) and the average speed of Tuna T5 was 5.1 km
h−1 (= 3.2 kn or 1.4 m s−1). The difference in travelling speeds may be due to the relatively small size
of Tuna T5 (~10 kg) compared to the tuna normally
associated with dolphins.
The dolphins and tuna showed different swimming patterns. The dolphin usually travelled during
the day at a depth of 15 to 20 m, in the mixed layer
above the thermocline. The characteristics of the
daytime dives (i.e. no rapid ‘wiggles’ or fluctuations at depth) suggested the dolphins were not
feeding (Bengtson & Stewart 1992, Testa et al. 1993,
Scott & Chivers 2009). The dolphins dove deeper at
night, often below the thermocline, apparently to
feed on organisms associated with the deep scattering layer until dawn (Scott & Chivers 2009). The
deepest dive was to 121 m.
The tuna showed a different pattern. During the
day, the tuna swam in the mixed layer to about the
depth of the thermocline at 35 to 40 m, below the
typical swimming depths of the dolphins. After
dusk, when the dolphins began to dive deeper, the
tuna ascended to depths of about 25 m or less.
Near dawn, the 2 species showed strikingly different changes in swimming depths. As the dolphins
resumed their daytime swimming depth nearer the
surface, the tuna descended toward the thermocline. The greatest swimming depth of the tuna
was 110 m.
Fig. 2. Stenella attenuata and Thunnus albacares. Sample of vertical movements of Tuna T1 (yellow) and Dolphin D8 (orange)
simultaneously tracked during 21 to 22 November 1993. The depth of the thermocline is represented as a blue band
Mar Ecol Prog Ser 458: 283–302, 2012
288
TROPHIC INTERACTIONS
Methods
Stomachs from dolphins and yellowfin tuna were
sampled at sea by observers of the Inter-American
Tropical Tuna Commission (IATTC) during 1992 to
1994. The tuna and dolphins were caught by tuna
purse-seiners of the international fleet. For dolphin
sets in which 3 or more dolphins were sampled (to ensure a large enough sample size of prey items eaten
by the dolphins in that herd), samples were taken
from up to 25 dolphins and 25 yellowfin tuna. Each
animal was measured, the sex determined, and the
stomach and a core of dorsal muscle were collected
and frozen for food habits and for stable isotope analysis (Román-Reyes 2005), respectively. On occasion,
the tunas were marked immediately after capture,
placed in the vessels’ fish holds, and sampled after
unloading.
In the laboratory, the stomach samples were thawed,
and stomach fullness, as a percentage of stomach
capacity, was estimated visually. The stomach contents were identified to the lowest taxon possible,
weighed, and counted (Galván-Magaña 1999), and
degree of digestion was determined (Olson &
Galván-Magaña 2002). The data were stratified by the
local time of day that the sets began: 06:00−08:59 h,
09:00−11:59 h, 12:00−14:59 h, and 15:00−18:00 h.
Within each time stratum, the percent occurrence of
prey items that were fresh or in intermediate digestion state (‘Recent,’ digestion states 1 and 2 defined
by Olson & Galván-Magaña 2002) was calculated.
Two stomach fullness strata were calculated for each
time period. The ‘Full’ category comprised the percentage of predators whose stomachs were estimated
to be 50 to 100% full of food, and the ‘empty’ category comprised the percentage of predators that had
empty stomachs or contained only residual hard parts
that could have been consumed on a previous day.
Prey composition in stomach contents was analyzed both by prey weight and prey occurrence
because these diet indices emphasize different information about the diet of predators (Chipps & Garvey
2007). For each predator species (dolphins or tuna),
the proportional composition by weight of each prey
type in each individual was computed and averaged
for each prey type over all individuals with food
remains in the stomachs during the entire day, as:
⎛
⎞
⎜
⎟
W
1
ij
⎟
MWi = ∑ ⎜ Q
P j =1 ⎜
⎟
W
⎜⎝ ∑ ij ⎟⎠
i =1
P
(1)
where MWi is mean proportion by weight for prey
item i, Wij is the weight of prey item i in stomach j, P
is the number of individuals with food in their stomachs, and Q is the number of prey types in the sample
(Chipps & Garvey 2007). Digestion-resistant hard
parts (squid mandibles and fish otoliths) were disregarded to ensure that only recent prey items were
included. The occurrence-based prey composition
(percentage of all individuals sampled whose stomachs contained a particular prey species) included
residual hard parts to provide a longer-term view of
the diet, although this may include periods of time
when the tuna and dolphins were not associated. The
prey were grouped into categories according to their
taxonomy and whether the species remained in the
epipelagic zone day and night or migrated vertically
into the zone at night.
Results
Data were analyzed from the 73 sets that had a
sample size of at least 3 yellowfin tuna stomachs and
at least 3 spotted and/or spinner dolphin stomachs.
The 73 sets provided samples from 218 spotted dolphins, 172 spinner dolphins, and 1523 yellowfin tuna
that were spatially distributed across the geographical range of the fishery (Fig. 3). Sets were made during daylight, with the earliest set at 07:55 h and the
latest set at 18:06 h. Prey remains, excluding residual
hard parts, were found in the stomachs of 23% of the
spotted dolphins, 17% of the spinner dolphins, and
64% of the yellowfin tuna. The principal taxa are
listed in Table 2.
The daily trends in digestion state and stomach fullness illustrate the difference in the feeding times of
the dolphins and the tuna (Fig. 4). Most of the spotted
and spinner dolphins had full stomachs when caught
during the early morning, but the percentages with
full stomachs and recently eaten prey declined and
percentages with empty stomachs increased throughout the day (Fig. 4). Full stomachs and signs of recent
feeding were rare in the afternoon for both dolphin
species. The yellowfin tuna, however, showed signs of
recent feeding and full stomachs throughout the daytime, with the greatest percentage of empty stomachs
occurring in tuna caught in early morning sets
(06:00−08:59 h). Thus, the digestion and fullness data
indicate that the dolphins feed mainly at night and in
the early morning, whereas the tuna feed throughout
the daylight hours but less at night.
Differences in the mass of prey in the stomachs
confirmed that the dolphins fed primarily at night.
Scott et al.: Tuna–dolphin association
289
The prey weights per stomach sampled were (mean ± SE) 29 ± 6 g for
spinner dolphins, 101 ± 12 g for spotted
dolphins, and 254 ± 11 g for yellowfin
tuna. The observed prey weights for
the spotted dolphins were only 1 to 8%
of what would be expected; an energetics study (Edwards 1992) estimated
that the foraging requirement of spotted dolphins is 5 to10 times that of yellowfin tuna. This large discrepancy
between the observed prey weights
for spotted dolphins and that expected
based on the Edwards energetics model
indicates that daytime sampling underestimates their prey consumption.
Fig. 3. Stenella attenuata, S. longirostris, and Thunnus albacares. Locations
The weight-based measure of prey where stomach samples were collected by IATTC observers aboard purse
seiners during 1992 to 1994
composition indicated that spotted dolphins consumed most of their daily rations during the night and early morning. Forty-three
The occurrence-based measure of prey composipercent of the food in the stomachs of spotted
tion also indicated different feeding times for the doldolphins during the entire daytime was from animals
phins and tuna. Stomachs from both dolphin species
captured between 06:00 and 08:59 h. Prey composilargely contained the remains of vertically migrating
tion was dominated by vertically migrating cephaloprey at all times of the day. The vast majority of these
pods and epipelagic flyingfishes, scombrids, noprey remains were digestion-resistant squid manmeids, and crustaceans (Fig. 5). Spinner dolphins
dibles and fish otoliths, which accumulate in the
fed mainly on vertically migrating myctophid fishes
stomachs. For spotted dolphins, the diurnal pattern
(Fig. 5). Daytime feeding by spinner dolphins was
of prey occurrence supported the weight-based data
rare; 81% of the food in spinner dolphins’ stomachs
in that the high prey diversity, which included
during the entire daytime was from animals captured
epipelagic taxa in the early morning, declined in the
between 06:00 and 08:59 h. In contrast, yellowfin tuna
afternoon. For spinner dolphins, virtually all occurpreyed largely on epipelagic fishes; prey that vertirences of cephalopods and fishes in the stomach
cally migrates to near-surface waters at night comcontents were animals eaten earlier and already
prised only minor percentages of the diet. Scombrids,
digested, with only hard parts remaining. For yellowparticularly frigate tunas Auxis spp., dominated the
fin tuna, epipelagic prey were important in occurfresh food remains during the daytime (Fig. 5).
rence throughout the day, although mesopelagic
Table 2. Stenella attenuata, S. longirostris, and Thunnus albacares. Categories of prey remains in the stomach contents of spotted dolphins (Sa), spinner dolphins (Sl), and yellowfin tuna (Ta), and the principal prey based on percent mass in each category
Category
Order (O) or Family (F)
Vertical migrating
Cephalopods
Fishes
Ommastrephidae (F)
Phosichthyidae (F)
Epipelagic
Cephalopods
Teuthoidea (O)
Argonautidae (F)
Exocoetids
Hemiramphidae (F)
Exocoetidae (F)
Scombrids
Scombridae (F)
Nomeids
Nomeidae (F)
Other epipelagic fishes Ostraciidae (F)
Crustaceans
Galatheidae (F)
Portunidae (F)
Species
Common name
Predator
Dosidicus gigas
Vinciguerria lucetia
Jumbo or Humboldt squid
Lightfish
Ta, Sa
Ta, Sl
Thysanoteuthis rhombus
Argonauta spp.
Oxyporhamphus micropterus
Exocoetus volitans
Auxis spp.
Cubiceps pauciradiatus
Lactoria diaphanum
Pleuroncodes planipes
Euphylax robustus
Diamondback squid
Ta
Argonauts
Ta
Bigwing halfbeak
Ta, Sa
Tropical two-wing flyingfish Sa, Ta
Frigate and bullet tunas
Sa, Ta
Driftfish
Ta, Sl, Sa
Boxfish
Ta
Pelagic red crabs
Ta
Swimming crabs
Ta
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Fig. 4. Stenella attenuata, S. longirostris, and Thunnus albacares. Percentages of predators whose stomachs were estimated to be 50 to 100% full (‘Full’) and stomachs that had
no fresh remains (‘Empty’), and percent occurrence of all
prey items, including residual hard parts, in digestion states
1 and 2 (‘Recent’). The data were stratified by time of
day that the sets were initiated: 06:00−08:59 h (10 sets),
09:00−11:59 h (14 sets), 12:00−14:59 h (28 sets), and
15:00−18:00 h (21 sets). The sum of the percentages of Full
and Empty stomachs is less than 100% because those with
fullness > 0 to 49% are not displayed
Fig. 5. Stenella attenuata, S. longirostris, and Thunnus albacares. Percentage composition by weight (see Eq. 1) of
each prey type in each individual tuna or dolphin averaged
for each prey type over all tuna or dolphins with food remains in the stomachs during the daytime (06:00−18:00 h).
Error bars are 2 SE from the mean. The data for residual
hard parts were omitted
Scott et al.: Tuna–dolphin association
cephalopods were also high in occurrence during the
daytime after 09:00 h, which is likely due to residual
mandible retention (81 to 94% of the records were
hard parts).
SPATIAL ASSOCIATIONS
Methods
IATTC or national observer programs have monitored virtually 100% of the large tuna purse-seiners
fishing in the ETP since 1992. These observers collect
information on dolphin sightings, tuna catches, mortalities of dolphin and other bycatch species, and
other data (Bayliff 2001). Dolphin sighting and dolphin set data from 1995 to 2005 were stratified by 5°
quadrat for pure herds of spotted and spinner dolphins and mixed-species herds of these 2 species.
Data were included only if the purse-seiner had
made at least one dolphin set during the cruise. The
data base included trips monitored by observers from
the IATTC (all years) and the national programs of
Venezuela (2000 to 2005), Ecuador (2001 to 2005),
and Colombia (2005). Data from the Mexican national program that monitors half of the Mexican fleet
were, however, not available for this study.
The percentage of sets-to-sightings was used as an
index of the prevalence of the tuna-dolphin association. Sightings included those made and identified
as pure and mixed herds of offshore spotted and
spinner dolphins by either the observer, or the shipboard or helicopter crew members.
Because data requiring identification of dolphin
species by crew members were used in these calculations, only the 2 species that the crews were most
familiar with, spotted and spinner dolphin, were considered. There are also caveats about the use of the
index. The index likely overestimates the prevalence
of the association because some dolphin sightings by
the crew may not have been reported to the observer
when no tuna were present, and this bias may have
increased somewhat since the 1980s (Lennert-Cody
et al. 2001). Another potential cause of overestimation is that small herds of dolphins are less likely to
be detected and less likely to carry tuna than larger
herds. However, we found no significant interannual differences in the index for the 1995 to 2005
time period chosen. We included only those quadrats
where sightings of either of the 2 dolphin species
were recorded by the purse-seiner observers, indicating that the quadrat was within the distributional
ranges of both the dolphins and fishery.
291
Using a linear regression, the tuna-dolphin association index for each 5° quadrat was modeled as a
function of the 1995 to 2005 average mixed-layer
depth for the corresponding quadrat. The mixed layer
depth (the depth at which temperature equals the sea
surface temperature minus 0.8°C) was calculated
from the Simple Ocean Data Assimilation model
(Carton et al. 2000) and served as a proxy for both the
depth of the thermocline and the upper boundary of
the oxygen minimum zone. The annual average
mixed-layer depth was used for most quadrats, but
for some quadrats, where the fishery only occurred
in a few months of the year, 1 or 2 quarterly averages
were used instead to match the months in which the
dolphin sightings were recorded.
Results
The percentage of single-species sightings that led
to sets (indicating tuna were likely present) was 42%
for spotted dolphins (39 593 sets in 94 202 sightings);
the percentage ranged as high as 73% but declined
to less than 30% where the mixed layer depth deepened to over 40 m. The average for spinner dolphins
was only 20% (3159 sets in 15 888 sightings); the percentage ranged as high as 46% but declined to 15%
or less where the mixed layer depth deepened to
over 30 m. Mixed herds of spotted and spinner dolphins had the highest percentage with 54% (32 094
sets in 59 778 sightings). The higher percentage for
mixed herds is likely due to these herds tending to be
larger than single-species herds and larger herds
tending to be more attractive to fishermen because
they yield larger catches of yellowfin tuna (Scott &
Cattanach 1998, Perkins & Edwards 1999).
The mixed layer is very shallow in the eastern tropical Pacific, but deepens to the west (Fig. 6). A linear
regression of the association index on mixed layer
depth showed significant trends for pure herds of
spotted (p < 0.01) and spinner dolphins (p < 0.01), and
for mixed spotted-spinner dolphin herds (p = 0.01).
The association between tuna and dolphins increased
as the mixed-layer depth shallowed.
For spotted dolphins, the association is most prevalent in waters where the depth of the mixed layer is
about 45 m or less (Figs. 6 & 7), and the oxygen concentration below the mixed layer is extremely low.
The spatial pattern of mixed spotted-spinner herds
was similar to that of spotted dolphins. Pure spinner
dolphin herds are not thought to normally carry tuna
(unless spotted dolphins are also present). However,
there are areas where the association with tuna is
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position to associate with objects. This
could serve as a mechanism to increase
their own encounter rates and facilitate
school formation (Fréon & Misund
1999, Fréon & Dagorn 2000). These authors have suggested that tuna–dolphin aggregations may represent a
specific version of the ‘meeting point’
phenomenon whereby the dolphin
school, while mobile, provides a cue
that allows yellowfin tuna to aggregate
into larger schools.
Two main hypotheses to explain why
tuna and dolphins associate propose (1)
benefits due to increased foraging effiFig. 6. Average annual mixed layer depths (in m) during 1995 to 2005 (adapted ciency, or (2) benefits from reduced risk
from Fiedler & Talley 2006). Note that the depth of the mixed layer, represent- of predation. To fully explain the assoing the top of the thermocline, is shallowest (blue) in the eastern tropical Pacific ciation we must determine which speand deepens to the west (yellow)
cies initiates the association and
whether the association is obligatory or
relatively strong—areas where the depth of the mixed
facultative for one or both species. The hypothesis
layer is about 25 m or less (Figs. 6 & 8), with a hypoxic
must explain not only the benefits of the association,
oxygen minimum zone below.
but why yellowfin tuna associate primarily with spotDistribution plots of sets on tuna associated with
ted dolphins, to a lesser extent with spinner dolphins
spotted and spinner dolphins show that the spatial
and common dolphins, and rarely, if ever, with the
extent of the tuna–dolphin association changes seaseveral other species of dolphins occurring in the ETP;
sonally. For the spotted dolphin, there are areas
why this association involves primarily large yellowfin
along the northern and southern margins of the distuna and not small yellowfin or other tunas; and why
tribution where the association is prevalent only in
dolphins and tuna associate in the ETP and only to a
the summer (Fig. 7), while for the spinner dolphin, a
much a lesser degree, if at all, in other oceans.
southern cluster of sets is present only in the austral
summer (Fig. 8). This expansion in the distribution of
dolphin sets coincides with the summer shallowing of
Which species follows the other?
the mixed layer, particularly north of 20° N and south
of 15° S (Fiedler 1992). This seasonal pattern is illusThis is not as simple a question as it may appear
trated in a 5° quadrat (85 to 90° W, 10 to 15° S) where
because there are no obvious ‘leaders’ or ‘followers’
the seasonal differences in dolphin sets were particin the spatial sense — one species or one individual is
ularly dramatic; sets occurred only when the average
not always in front of the aggregation and the species
depth of the mixed layer was at a minimum (Fig. 9).
that initiates the association may not be obvious. In
the constantly shifting aggregations of tuna and dolphins, individuals or species in front of the aggregaDISCUSSION
tion at one moment will find themselves on the flank
or rear of the aggregation when it changes direction.
Tunas are known to associate often with floating
Early observations by baitboat fishermen (Silva 1941)
objects, whale sharks, whales, and dolphins (see resuggested the tuna followed the dolphins, but others
views in Scott et al. 1999). In the ETP, small tunas are
(Godsil 1938) suggested the opposite. Most fishercommercially caught in association with floating obmen, however, have come to believe that the tuna
jects or as free-swimming (unassociated) schools, but
follow the dolphins (National Research Council 1992,
large yellowfin tuna are usually caught in association
Felando & Medina 2011). They consistently observed
with dolphins. A ‘meeting place’ hypothesis has been
that if the dolphins moved away from the baitboat,
proposed that links the associations of small tunas
the tuna would follow, even while the fishermen
and floating objects and large yellowfin tuna with
were chumming the water with live baitfish. When
dolphins by arguing that tunas have a genetic predisthe purse-seine fishery began, the fishermen ob-
Scott et al.: Tuna–dolphin association
293
ability to echolocate and find prey
patches at a distance. Scientists observing underwater behavior inside
the purse-seine net suggested that the
tuna follow dolphins (Norris et al.
1978, Pryor & Kang 1980). Mathematical population models have indicated
that the species with the shorter lifespan, the tuna, must benefit if the association is to remain stable (Mullen
1984). Comparative bioenergetics models suggested that it is unlikely that
dolphins initiate the association because the dolphins have greater foraging requirements (Edwards 1992).
Is the association obligatory or
facultative?
Yellowfin tuna and spotted dolphins
are both found throughout the tropics
but only have a persistent, spatially extensive association in the ETP, so it is
not likely that the association is obligatory for either species. The tracking
results supported this: even though
Tuna T1 and Dolphin D8 were caught
and released together, they separated
shortly afterwards and T1 did not join
other dolphin herds that were sighted
about 400 m away. A previous tracking
study of yellowfin tuna in the ETP also
showed that tagged tuna sometimes
joined nearby herds of spotted dolphins
and at other times did not (Carey & Olson 1982). A study of dolphin and tuna
group sizes found that spotted and
Fig. 7. Stenella attenuata and Thunnus albacares. Sets on tuna associated with
spinner dolphin herds and yellowfin
pure herds of spotted dolphins from 1995 to 2005 during April to September
and October to March
tuna schools all increased in numbers
during the day and fragmented at
served that successfully herding the more-visible
night (Scott & Cattanach 1998). The nighttime fragdolphins reliably yielded catches of tuna, whereas
mentation of both dolphin and tuna aggregations led
when even a small part of the dolphin herd escaped,
the authors to suggest that the tuna–dolphin associathe tuna often followed them out of the net and
tion weakened at night as well.
escaped as well (National Research Council 1992).
Researchers have also proposed different ideas
about which species initiates the association. Au &
What are the benefits of the tuna–dolphin
Pitman (1986, 1988) suggested that the tunas’ ability
association?
to drive prey to the surface attracts seabirds and
could attract the behaviorally adaptable dolphins as
In the light of the results of our 3 studies, we rewell, while Norris et al. (1994) argued that it would be
examine the 2 hypotheses put forward previously.
advantageous for the tuna to exploit the dolphins’
It has often been suggested that there is not a
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Foraging benefits
The results of Perrin et al.’s (1973)
food-habits study not only indicated
that there was overlap in the prey species eaten by spotted dolphins and yellowfin tuna, but provided evidence of
prey species specialization as well. Spotted dolphins and yellowfin tuna were
thought to feed primarily on epipelagic
prey, while spinner dolphins fed primarily on mesopelagic prey (see also
Fitch & Brownell 1968, Morán-Angulo
et al. 1995). The observation that tuna
associate more readily with spotted
dolphins than with spinner dolphins
led other authors to suggest that the
similarity in food habits is the basis of
the tuna-dolphin association and that
one or both of the species gains feeding benefits from the association (Norris
1978, Norris & Dohl 1980a, Au & Pitman
1986, 1988, Pryor & Kang-Schallenberger 1991, Au 1991, Edwards 1992,
Norris et al. 1994). However, the sample size (5 sets from which both dolphin and tuna stomachs were examined) in Perrin et al.’s (1973) study was
too small to detect feeding differences
between yellowfin tuna and spotted
dolphins by time of the day.
Food habits data collected in our
study from 73 sets in which tuna and
dolphins were caught together do not
support the feeding hypothesis. The
tuna–dolphin association is primarily a
diurnal one (Scott & Cattanach 1998)
and if the association was based on
Fig. 8. Stenella longirostris and Thunnus albacares. Sets on tuna associated
feeding benefits, one would expect
with pure herds of spinner dolphins from 1995 to 2005 during April to
both dolphins and tuna to feed primarSeptember and October to March
ily in the daytime. In the ETP, however, yellowfin tuna are primarily daysingle cause for the tuna–dolphin association, but
time feeders, while spotted and spinner dolphins are
rather a combination of factors (Hammond 1981,
primarily nighttime or crepuscular feeders (Reintjes
Au & Pitman 1988, Scott & Cattanach 1998, Fréon
& King 1953, Alverson 1963, Shomura & Hida 1965,
& Dagorn 2000). As with conspecific schools, the
Fitch & Brownell 1968, Perrin et al. 1973, Ortegasize of a mixed-species group is likely a result of
García et al. 1992, Buckley & Miller 1994, Perrin
the dynamic balance between the risk of predation
& Hohn 1994, Richard & Barbeau 1994, Roger 1994,
tending to increase group size for protection, and
Robertson & Chivers 1997, Fiedler et al. 1998, Scott &
prey distribution tending to limit groups to a size
Cattanach 1998, Galván-Magaña 1999, Románthat can be sustained by the available resources
Reyes 2005, this study). While yellowfin tuna may
(Jarman 1974, Janson & Goldsmith 1995, Scott &
also feed at night and both dolphin species feed occaCattanach 1998).
sionally during the day, daytime feeding is clearly
Scott et al.: Tuna–dolphin association
295
extend to multi-species aggregations,
whereby the combined number of individuals of all species dilutes the risk of
predation to individuals. Mixed-species
aggregations comprised of different
species with different sensory capabilities may also detect predators more
efficiently than either species could
provide alone (e.g. Diamond 1988).
Spotted dolphins and yellowfin tuna
are of a similar size and have the same
potential predators (Scott & Cattanach
1998). The predation risk may be particularly high for the yellowfin tuna beFig. 9. Stenella attenuata, S. longirostris, and Thunnus albacares. Number of
cause sharks and billfishes are signifisets from 1995 to 2005 made on tuna associated with pure herds of spotted
cant predators that are commonly caught
and spinner dolphins by month in one 5° quadrat (85 to 90° W, 10 to 15° S).
with tunas (Au 1991, Hunsicker et al.
Overlaid is the average mixed layer depth for that same quadrat by month
2012). Hunsicker et al. (2012) found that
more important for the tuna and nighttime feeding is
even large yellowfin tuna were prey for large sharks,
more important for the dolphins.
particularly in the ETP, and they suggested that
The food-habits study found that, while there is
yellowfin tuna should more properly be considered a
some overlap in the diets of spotted dolphins and
mesopredator rather than an apex predator.
yellowfin tuna, the prey resources were largely partiRare observations of shark attacks on spotted doltioned by time of day, prey species, and size (Galvánphins illustrate how vulnerable dolphins may be
Magaña 1999). Stable isotope analysis performed on
when the protection provided by being part of a herd
muscle samples from a subset of the predators anais disrupted. Leatherwood et al. (1973) reported oblyzed for food habits (Román-Reyes 2005) revealed
servations of shark predation on spotted dolphins
trophic overlaps of about 78% between yellowfin and
after the herd’s structure had been disrupted by fishspotted dolphins and between spotted and spinner
ing operations in the ETP. Maldini’s (1993) observadolphins, but only 57% between yellowfin and spintion of an attack of a tiger shark Galeocerdo cuvier on
ner dolphins. Despite similarity among δ15N values of
a juvenile spotted dolphin off Hawaii illustrated the
the predators, trophic-level overlap only requires feedhigh predation risk faced by calves and juveniles and
ing on prey from overlapping trophic levels, and can
the vulnerability of dolphins when they stray outside
occur without sharing any of the same prey species.
the envelope of the herd. Successful attacks by
The tracking data also suggested that the yellowfin
sharks were typically ambushes initiated from behind
tuna and spotted dolphins feed at different depths.
and below the dolphin.
Although the hypothesis that the association is largely
Our results are in line with the expectations of the
food-based is not supported by current evidence,
‘meeting point’ hypothesis proposed to explain the
there may still be a foraging benefit. Both dolphin and
schooling of pelagic tunas (Fréon & Misund 1999,
tuna groups disaggregate during the night, beginning
Fréon & Dagorn 2000). The mobile dolphin herds
at dusk when dolphins begin to feed (Scott & Cattamay serve as a cue that allows tunas to aggregate
nach 1998, Scott & Chivers 2009). The feeding times of
into larger schools. At the same time, the benefit of
the spotted dolphins and yellowfin tuna overlap in the
‘safety in numbers’ is accentuated by the combined
dawn hours, however, and early morning feeding bouts
group size of 2 or more similarly sized species. Scott
on multi-species concentrations of prey may draw tunas,
& Cattanach (1998) noted that predation pressure
dolphins, and other predators into proximity, and thus
need not be high to promote these aggregations, only
serve as a catalyst in the creation of the association.
that the risk of predation should be less than that
incurred by an alternate strategy, such as forming
small groups or straying from the group in the presProtection from predators
ence of predators.
Large sharks are not only potential predators, but
Travelling in groups provides more protection from
competitors as well (Leatherwood et al. 1973, Compredation than travelling alone. This advantage can
pagne 1984, Heithaus 2001, Acevedo-Gutiérrez 2002,
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Maldini 2003). Pelagic sharks would be attracted to
the same prey patches as the dolphins and tuna, and
habitat compression would likely increase their
encounters. By monitoring each others’ alarm responses, the dolphins and tuna could both gain from
the association. The dolphins can echolocate or hear
predators at a distance, allowing them, and the associated tuna, to avoid or monitor the predators.
Because dolphins are most vulnerable to shark
attacks coming from behind and below (Cockcroft et
al. 1989, Mead & Potter 1990, Scott & Cattanach
1998), any alarm responses by deeper-swimming
tuna could alert the dolphins to predators beneath
them. Similarly, the surface-swimming spinner dolphins, which have been hypothesized to seek out
spotted dolphin herds to increase protection from
predation (Norris 1978, Norris & Dohl 1980b, Norris
et al. 1994, Cramer et al. 2008, Kiszka et al. 2011),
could also be alerted by the deeper-swimming spotted dolphins (discussed below).
Why does this association primarily involve spotted
dolphins, much more so than other dolphin species?
If the predation hypothesis is valid, it would require an explanation for why, if tuna join dolphin
herds seeking safety in numbers, do they associate
mainly with spotted dolphins, even though other species, particularly spinner and common dolphins, form
large herds that would provide protection as well.
The weaker association between yellowfin tuna
and common dolphins can be explained by their
different habitats. Yellowfin tuna are found primarily
in tropical waters, while common dolphins tend to
inhabit cooler, upwelling-modified waters (Au & Perryman 1985, Reilly 1990, Fiedler & Reilly 1994, Reilly
& Fiedler 1994, Ballance et al. 2006).
Spinner dolphins, however, inhabit tropical waters
and associate with yellowfin tuna, but generally as
part of a mixed-species spotted-spinner dolphin herd.
Spotted and spinner dolphin herds coalesce throughout the mornings such that, by mid-day, 87% of all
spinner dolphin sightings are in mixed-species herds
associated with spotted dolphins (Scott & Cattanach
1998). The apparent weaker association between yellowfin tuna and spinner dolphins may be explained,
in part, because tuna encounter pure spotted dolphin
herds and mixed spotted-spinner dolphin herds more
frequently than pure spinner dolphin herds. Thus,
even when tuna join pure spinner dolphin herds in
the early morning, it is likely that those herds will
soon coalesce with herds of spotted dolphins.
The tuna’s apparent preference for spotted dolphins can also be explained by their swimming
depths. The foraging depths of yellowfin tuna are
restricted by low dissolved oxygen concentrations,
and they cannot swim for long in waters where the
concentrations are less than 2.0 ml l−1 without resorting to ‘bounce diving’ (Schaefer et al. 2009). Tracking
studies (Carey & Olson 1982, Holland et al. 1990,
Block et al. 1997, Schaefer et al. 2007, 2009, this
study) have shown that yellowfin tuna are typically
found during the daytime near or slightly above the
thermocline (20 to 60 m deep in the ETP areas where
the association is most often observed and exploited
by the fishermen). Aerial photogrammetry studies
have observed that spinner dolphins are easier to
photograph than spotted dolphins (Cramer et al.
2008) because spinner dolphins swim near the surface while spotted dolphins swim deeper (W. Perryman & M. D. Scott pers. obs.); the TDR data confirmed
that the spotted dolphins swim at depth, travelling 15
to 20 m below the surface during the daytime. Radiotracking and aerial photogrammetry data also indicate that common dolphins, like spinner dolphins,
are also surface swimmers during the day (Evans
1974, W. Perryman & M. D. Scott pers. obs.). Thus,
the depth at which spotted dolphins typically swim is
much closer to the typical swimming depth of the yellowfin tuna than that of the spinner and common dolphins. It would be easier for the tuna, swimming just
above the thermocline, to maintain an association
with the deeper-swimming spotted dolphins than the
surface-swimming spinner dolphins.
If differences in swimming depth were indeed influencing the formation of the tuna–dolphin association, then one might expect tuna to associate with
spinner dolphins where the mixed layer was the
shallowest and the oxygen minimum zone just below
the mixed layer was most hypoxic. Comparison of the
mixed layer depth (Fig. 6) to the distribution of sets
on tuna associated with pure herds of spinner dolphins (Fig. 8) and with spinner dolphins in southern
areas during summer when the mixed layer depth is
shallower (Fig. 9) suggests that this is so.
Why does this association involve primarily large
and not small tunas?
The yellowfin tuna caught by purse seines in association with floating-object sets are small (averaging
2.6 to 4.6 kg, modal fork length [FL] ~45 cm, depending on area), those caught in unassociated schools
are larger (8.7 to 11.2 kg, modal FL ~70 cm), and
Scott et al.: Tuna–dolphin association
those caught in association with dolphins are the
largest (13.5 to 37.3 kg, modal FLs > 90 cm; IATTC
2004). Edwards (1992) argued that it would not be
energetically efficient for small yellowfin tuna or
skipjack to travel with dolphins until they reached at
least the same length of a newborn spotted dolphin
(about 85 cm, Hohn & Hammond 1985; or a weight of
about 12.9 kg, Wild 1986). Otherwise, Edwards (1992)
argues, smaller tunas would have to travel faster than
their optimum cruising speed to keep up with the
dolphins, which is energetically unsustainable. When
small tunas are associated with dolphins, they do
comprise a small proportion of the catch, likely because they may not be able to keep pace during the
high-speed chase that usually precedes a dolphin set.
Why is the association of dolphins and tuna such a
predominant feature in the ETP, but not in most
other oceans?
It has long been suggested that the unusual
oceanographic features of the ETP— the high surface
temperatures, shallow thermocline (< 60 m deep),
and the thick oxygen minimum zone — promotes the
association of tuna and dolphins (Green 1967, Perrin
et al. 1976, Au & Perryman 1985, Edwards 1992, Norris et al. 1994). Oxygen is depleted in warm waters of
the mixed layer due to high phytoplankton production, and the stable thermocline prevents oxygenation of the cooler waters below, producing the characteristic thick oxygen minimum zone (see review by
Fiedler & Talley 2006). The oxygen minimum zone in
the ETP ‘includes a greater body of almost oxygenfree water than any other region in the world’s
oceans’ (Knauss 1963). To the west, the thermocline
deepens to about 150 m and the oxygen minimum
zone thins markedly (Knauss 1963, Sprintall &
Cronin 2001, Tomczak 2001), and the tuna–dolphin
association becomes uncommon. Tuna purse seiners
in the western Pacific rarely set on dolphins (Donahue & Edwards 1996, Hall 1998, Hampton & Bailey
1999, WCPFC 2011).
The combination of a shallow thermocline and a
thick layer of cold hypoxic water just below is
thought to restrict the vertical movements of tunas
(Edwards 1992, Brill 1994, Prince & Goodyear 2006).
Although yellowfin tuna may make occasional dives
down into very cold water (Carey & Olson 1982,
Block et al. 1997, Dagorn et al. 2006), their vertical
range appears to be limited by temperatures that are
about 8°C less than the surface temperatures (Brill &
Lutcavage 2001) and by an oxygen content of about
297
3.5 ml l−1 or 152 µmol kg−1 (Cayré 1991, Cayré and
Marsac 1993, Brill 1994, Graham & Dickson 2004,
Prince & Goodyear 2006).
This compresses the yellowfin tuna habitat to the
surface waters of the mixed layer and allows the
tuna–dolphin association to occur. Yellowfin tuna
tend to swim just above the thermocline, with frequent excursions upward within the mixed layer
(Carey & Olson 1982, Holland et al. 1990, Block et al.
1997, Brill et al. 1999, this study); the air-breathing
spotted dolphins are obviously tied to the surface,
and spend most of their time in the mixed layer travelling and foraging. The shallow thermocline also
promotes propagation of dolphin sounds, and yellowfin tuna may detect these sounds at distances of
several hundred meters (Finneran et al. 2000, Schaefer & Oliver 2000). The deeper the thermocline, however, the greater the vertical distance there is
between the 2 species, and the more difficult it would
be to maintain the association. This would explain
why the association is so prevalent in the ETP and
then becomes progressively rarer farther to the west.
It may also explain the effects on tuna catches during
some El Niño years. During the severe 1983 El Niño,
for example, the mixed layer in the ETP deepened
over a wide area, and likely as a result, made the
tuna–dolphin association more difficult to maintain,
which likely explains the greatly reduced number of
dolphin sets and tuna catches in that year (Fig. B-4 in
IATTC 2004).
The association between dolphins and tuna is not
entirely unique to the ETP, however. Tuna associate
with dolphins around many islands: the Maldives
(Anderson & Shaan 1999), Sri Lanka (de Silva & Boniface 1991, Leatherwood & Reeves 1991), Fernando
de Noronha Archipelago (Sazima et al. 2006), the
Azores (Clua & Grosvalet 2001, Silva et al. 2002),
Hawaii (Shallenberger 1981), and the Philippines,
Indonesia, and New Guinea (Dolar 1994, Hampton &
Bailey 1999, WCPFC 2011). These associations may
be promoted by the shallower thermocline in the lee
of some islands (e.g. McManus et al. 2008). Dolphins
and tuna are also known to associate, to a much
lesser extent than in the ETP, in the tropical waters of
the western Indian and the eastern Atlantic Oceans
(Simmons 1968, Levenez et al. 1980, Pereira 1985,
Donahue & Edwards 1996, Ballance & Pitman 1998,
Hall 1998, Ariz-Telleria et al. 1999, Van Waerebeek
et al. 1999, Felando & Medina 2011). These ocean
regions contain areas with a shallow thermocline and
a marked oxygen minimum zone (Fig. 10), although
these areas are not as expansive nor is the oxygen
minimum zone as hypoxic as in the ETP (Tomczak
Mar Ecol Prog Ser 458: 283–302, 2012
298
Fig. 10. Global minimum dissolved oxygen concentration (µmol kg–1) from World Ocean Atlas 2001 (adapted from Fiedler &
Talley 2006). Letters indicate approximate areas where published accounts refer to a tuna–dolphin association: (A) Gulf of
Oman and Arabian Sea: Van Waerebeek et al. (1999), Ballance & Pitman (1998); (B) Sri Lanka: de Silva & Boniface (1991),
Leatherwood & Reeves (1991); (C) Archipelagic waters of Indonesia, Philippines, and New Guinea: Dolar (1994), Hampton
& Bailey (1999), WCPFC (2011); (D) Hawaiian Islands: Shallenberger (1981); (E) Eastern tropical Pacific: Figs. 7 & 8; (F)
Fernando de Noronha archipelago: Sazima et al. (2006); (G) Azores Islands: Clua & Grosvalet (2001), Silva et al. (2002);
(H) Gulf of Guinea: Simmons (1968), Levenez et al. (1980)
2001, Prince & Goodyear 2006, Prince et al. 2010).
Only in the ETP is the association strong enough and
reliable enough for a pelagic commercial purse-seine
fishery to take advantage of the association consistently (Donahue & Edwards 1996, Hall 1998, Scott et
al. 1999).
CONCLUSIONS
The ‘meeting point’ hypothesis (Fréon & Misund
1999, Fréon & Dagorn 2000) proposes that tuna have
a genetic tendency to associate with floating objects,
dolphins, whales, or whale sharks. Observations by
fishermen and studies by researchers have provided
evidence that it is the yellowfin tuna that initiates the
association with dolphins. Our results, however, suggest that the tuna–dolphin association is neither an
obligatory nor a permanent one. It involves mainly
large yellowfin tuna, and not small yellowfin or skipjack tunas, likely due to energetic constraints on
small tunas (Edwards 1992). It involves mainly spotted dolphins, and only to a lesser extent other dolphin
species, due to the closer match in habitat and travelling depths of the spotted dolphins with the yellowfin
tuna. The association is most common in the ETP
because this large region is characterized by warm
waters and a shallow thermocline overlaying a thick
hypoxic oxygen minimum zone that compresses the
habitat for the tuna (Prince & Goodyear 2006). The
shallower the thermocline and the more hypoxic the
waters below the thermocline, the more likely it is
that the association will occur.
The results of our studies support the hypothesis
that the formation of large, mixed-species groups of
spotted dolphins and yellowfin tuna reduces the risk
of predation for one or both species. Both species
show increased group sizes during the day, likely for
the same reason, as both are potential prey for large
sharks and small whales (Scott & Cattanach 1998).
The habitat compression that promotes the tuna–
dolphin association may also increase the number of
encounters with sharks. Large sharks are both potential predators on and competitors with dolphins and
tuna. All of these species are likely attracted to the
same prey patches, particularly during early morning
feeding bouts. The dolphin–tuna association may
then be maintained throughout the day because of
the threat sharks pose as potential predators.
Acknowledgements. This research has been based on a scientific foundation built by many people, over many decades,
and covering many disciplines. Many of the insights in this
study were influenced by the observations of fishermen and
the research of R. Allen, D. Au, R. Brill, L. Dagorn, E.
Edwards, F. Galván-Magaña, M. Hall, P. Hammond, A.
Hohn, K. Norris, E. Prince and P. Goodyear, S. Reilly, W. Per-
Scott et al.: Tuna–dolphin association
rin and his many colleagues, and W. Stuntz. Many of these
colleagues have sharpened our ideas during many discussions over the years. Commander D. Peterson and the crew
of the RV ‘McArthur’ provided support, advice, and encouragement to safely conduct our tagging and tracking operations. The crew integrated themselves into every facet of the
research: tagging and tracking dolphins and tuna, logistical
support, scientist-overboard recovery, and collecting environmental data. The purse seiner ‘Convemar’ was chartered
by the IATTC and the Programa Nacional para el Aprovechamiento del Atún y Protección de los Delfines of Mexico.
Captain B. Cervantes and the crew of the ‘Convemar’
helped in the safe capture, release, and tracking of the dolphins and tuna. We thank the small army of people from the
IATTC, NMFS, and NOAA Corps who supported the project
logistically. We also thank the biologists who accompanied
us in the field: G. Aldana, W. Armstrong, J. Asch, D. Bratten,
M. García, J. Ramírez, H. Rhinehart, and B. Wetherbee. The
stomach and muscle-tissue samples were collected by
IATTC observers, and the stomach contents were processed
by F. Galván-Magaña and J. Martinez. The stable isotope
samples were analyzed by J. Román-Reyes. We thank them
and the many IATTC staff members who participated in the
training and logistics of the trophic relations study. The data
for the spatial study of the fishery were collected by observers of the IATTC and of national programs, N. Vogel
performed the ‘data extraction from Hell’ to assist in the
analyses, and R. Allen and C. Patnode created the illustrations. The manuscript was reviewed by B. Bayliff, R. Deriso,
C. Lennert-Cody, W. Perrin, W. Perryman, G. Watters, and 3
anonymous reviewers.
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Submitted: December 22, 2011; Accepted: April 2, 2012
Proofs received from author(s): June 17, 2012